Spatiotemporal changes in TFL1 gene expression as a main driver of Asteraceae capitulum evolution

The Asteraceae constitutes one of the most diverse and widespread plant families on Earth. The evolutionary success of the family has been attributed to its unique inflorescence structure, known as the capitulum. Concerning its evolutionary origin, two prevalent hypotheses have been proposed. The so-called flower unit meristem (FUM) hypothesis assumes a single-step evolution at the inflorescence meristem (IM) level to mimic a solitary flower, whereas the inflorescence hypothesis proposes gradual evolution in general inflorescence architecture among the Asteraceae and its sister families. Our previous results indicate a potential role for TERMINAL FLOWER 1 (TFL1) in divergence between the inflorescence architectures of Asteraceae and its sister family, Calyceraceae. This study combines gene expression profiling with morphological and histological analysis to clarify the two compelling hypotheses. Comparative expression analysis of TFL1 homologues revealed differences in their spatiotemporal expression dynamics during early IM development between Gerbera hybrida and Acicarpha tribuloides, two representative species of Asteraceae and Calyceraceae. Specifically, I discovered that GhTFL1 exhibits prolonged expression corresponding to the rapid expansion phase of Gerbera IM, in contrast to AcTFL1a and AcTFL1b genes, whose expression was absent after the vegetative-to-reproductive transition of the meristem. Furthermore, by conducting detailed anatomical analysis of developing Acicarpha IMs, as well as of Gerbera lines (wild type, transgenic GhTFL1 overexpression, RNAi), I revealed that their meristem growth dynamics and histological configurations differ considerably. Instead of forming a broad and flattened meristem (observed in wild-type and 35S:GhTFL1 line), the RNAi-GhTFL1 line developed a narrow, elongated meristem resembling that of Acicarpha that forms a defining terminal flower. In support of the inflorescence hypothesis, the results suggest that changes in TFL1 gene expression dynamics may have driven the divergence between Asteraceae capitulum and Calyceraceae cephalioid. Future functional studies elaborating Acicarpha as a new model for Calyceraceae would help to validate these findings further.